Off-season survival and life history of beet armyworm, Spodoptera exigua (Hubner) on various host plants

The beet armyworm, Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae), has become a significant pest of chickpea in recent years. The polyphagous nature allows it to survive on various hosts during the off-season, creating a great menace to the crop in the following season. To assess the incidence and document the alternate hosts of S. exigua, a rapid roving survey was conducted in 11 chickpea-growing areas of Prakasam district, Andhra Pradesh, India. Additionally, the life history traits of S. exigua were studied on major alternate host plants under laboratory conditions (27 ± 1 °C and 70 ± 2% RH) to understand the survival, life expectancy and potential contribution to future populations. The results show that, among the different crops surveyed, the maximum larval incidence was noticed in maize (1.93 larvae/plant), cowpea (1.73 larvae/plant), and sunflower (1.68 larvae/plant) during the off-season. Life history studies of S. exigua showed that highest larval survival percentage was observed on chickpea (83.6%), while the lowest was on maize (44.5%). The mean developmental time for larvae was longest on maize (27.1 days) and shortest on chickpea (14.9 days). Larvae did not develop beyond the third instar when fed with chilli. The growth index statistics showed chickpea (9.2) was the most suitable host plant, whereas maize (0.9) was the least suitable host. The age-stage-specific survival rate (Sxj) varied across developmental stages, and the survival curves overlapped, indicating different growth rates among individuals. The life expectancy (exj) at age zero was highest on groundnut (37.06 days). The intrinsic rate of increase (r) of S. exigua was lowest on maize (0.10 ± 0.0013) and highest on chickpea (0.22 ± 0.0010). Similarly, the net reproductive rate (R0) was highest on chickpea (846.39 ± 18.22) and lowest on maize (59.50 ± 2.06). The population doubled every 3.08 ± 0.011 days on chickpea compared to 7.22 ± 0.80 days on maize. The study conclusively indicates that chickpea and sunflower, primarily cultivated during the rabi season in India, are the most preferred hosts for S. exigua. In contrast, maize and cotton, mainly grown during the kharif season, are less preferred and merely support the pest's survival. Consequently, S. exigua switches hosts between different crops growing seasons, so effective management of S. exigua during the kharif season can help prevent pest outbreaks during the rabi season.


Incidence of S. exigua on different crops and weeds
The results of the field survey conducted in Prakasam district of Andhra Pradesh, show that the larvae of S. exigua were found to feed on 15 plant species, including two weed species.The off-season survey data revealed that the survival of S. exigua larvae varied between 0.5 to 1.93 larvae per plant, while leaf damage ranged from 3.94 to 37.92% (Table 1).During the off-season of 2016-2017, significant variations were observed in the incidence of S. exigua on various crops, including pulses (such as greengram, blackgram, cowpea, and soybean), oilseeds (groundnut, castor, and sunflower), commercial crops (chilli and cotton), vegetables (onion and brinjal), other crops (maize and tobacco nurseries), and weeds (wild amaranthus and Euphorbia geniculata) across the 11 mandals surveyed.Among the different crops examined, the highest larval incidence was observed on maize (1.93 larvae per plant), cowpea (1.73 larvae per plant), sunflower (1.68 larvae per plant), and groundnut (1.47 larvae per plant) during the off-season of chickpea cultivation (both pre and post Rabi season).In contrast, minimal larval populations were found on the alternate weed hosts E. geniculata and wild Amaranthus, with only 0.22 and 0.24 larvae per plant, respectively.Sunflower exhibited the highest percentage of leaf damage (37.92%), followed by cowpea (34.41%), groundnut (32.72%), and tobacco (30.13%), while E. geniculata showed the lowest damage at 3.94%.Similarly, the visual leaf damage rating was highest for sunflower (4.69) and lowest for E. geniculata (1.29).

Life history of S. exigua on different host plants
The results of the development period (Table 2), adult longevity (Table 3), and life span of S. exigua (Table 4) reared on different host plants are presented here.The duration of the egg incubation period differed among the host plants, with cotton exhibiting the longest period (3.5 days), whereas chilli showed the shortest incubation period (2.7 days) (Table 2).Host plants significantly influenced the percentage of egg hatch, with the highest observed on chickpea (92.7%) and the lowest on chilli (82.3%).Egg hatch rates on chickpea were comparable to those on groundnut (91.3%) and maize (90.2%).Significant variations in the duration of S. exigua larval instars were noted when reared on different host plants (Table 2).Overall, larvae exhibited faster development from the first to sixth instars when fed on chickpea (14.9 days).Chilli impeded larval development and growth, as evidenced by larvae failing to progress beyond the third instar and displaying prolonged developmental times during the first and second instars compared to other host plants studied.Regarding larval survival, the larvae reared on chickpea displayed the highest percentage (83.6%),while maize exhibited the lowest (44.5%).Notably, larvae did not survive on chilli (0%) under laboratory conditions, despite 82.3% of eggs successfully hatching into first instar larvae.There was a notable difference in the pupal period among the host plants.When larvae were fed on chickpea, the pupal duration of S. exigua was only 7.8 days, while larvae fed on maize showed a significantly longer pupal duration of 11.3 days (Table 2).Similar durations of the pupal stage were recorded in blackgram (8.7 days) and greengram (8.9 days).
There were notable differences in the pupal survival (adult eclosion) of S. exigua across various host plants.The survival rate on chickpea (84.8%) was significantly higher (P < 0.05) compared to other hosts.The percentage   2).Statistically significant differences (P < 0.05) in longevity were observed between male and female insects depending on the host plant.Male adults reared on groundnut (9.9 d) displayed significantly longer lifespan, as did females reared on blackgram with the most extended adult longevity (12.3 days) (Table 3).The longest oviposition period (9.0 days) was observed on castor, while the shortest was noted on maize (3.3 days).The highest fecundity was observed when the larvae were fed with chickpea, which had the highest number of total eggs laid per female during the larval stage (258.2eggs per female), while the lowest number of eggs laid was observed on maize (94.3 eggs per female).The pre-imaginal development period (41 days) and total lifespan (47.5 days) were significantly longer on maize (Table 4).However, the shortest pre-imaginal development period and total lifespan of the beet armyworm were on chickpea (25.7 and 35.3 days) and sunflower (28.6 and 35.8 days), respectively.Different host plants affected the survival of S. exigua till adulthood (P < 0.05), with the highest percent survival recorded when the larvae were reared on chickpea (70.9%) and the lowest on maize (9.9%) (Table 4).Table 5 displays the growth index and mortality percentages of larvae and pupae of S. exigua on various hosts.Chickpea demonstrated the highest growth indices for larvae and pupae, with values of 5.7 and 9.2, respectively.In contrast, the growth index of larvae and pupae on maize was 1.7 and 0.9, respectively, the lowest among all hosts.

Survival rate, life expectancy and reproductive value of S. exigua on different hosts
Age-stage-specific survival rate (S xj ) shows the probability that a newly laid egg of S. exigua survive to each agestage unit (Fig. 1).The figure represents survivor curve and stage differentiation among individuals of S. exigua reared on different hosts.The rearing of S. exigua on different hosts had a significant effect on the probability that a newly laid egg of S. exigua will survive to the adult stage.The values varied across developmental stages, and the survival curves were overlapped, which can be attributed to the fact that different individuals grow at different rates.The age-stage-specific life expectancy (e xj ) describes an expected lifespan of S. exigua individuals of age x and stage j on eight different hosts.The value of e xj showed a downward trend on all the hosts studied under the laboratory conditions, which indicate the life expectancy of the individual was reduced with the advancement of age (Fig. 2).The reproductive value (V xj ) of the S. exigua, indicates the contribution of a S. exigua individuals at age x and stage j to the future populations presented in Fig. 3.The age-specific survival rate (l x ), fecundity (m x ), and maternity (l x .mx ) values of S. exigua are shown in Fig. 4. The curve of l x is the pooled and simplified survival rate of S xj curves of different stages in Fig. 1, and it represents the probability that a newly laid egg will survive to      www.nature.com/scientificreports/while maize exhibited the longest doubling time (7.22 ± 0.80), reflecting their respective population growth rates.These results provide insights into the reproductive biology and population dynamics of these agricultural crops.

Discussion
Various characteristics of host plants, such as their quality, can impact the life cycle of herbivores, influencing factors like longevity, fecundity, and survival rates 9 .The presence of diverse host plants plays a crucial role in the population explosions of insects that feed on multiple plant species 8,13 .Research focusing on the biology and www.nature.com/scientificreports/establishment of life tables is essential for predicting future population trends and developing effective management strategies 19,20 .We conducted biological studies using detached leaves commonly employed in laboratory feeding experiments to provide accurate data.This approach helps reduce variability between individual plants and ensures a fair assessment of insect parameters such as consumption and development rates across different host plant species.Our findings, consistent with previous studies utilizing whole plants, suggest no significant disparities in the population dynamics and growth parameters of S. exigua 21,22 .Consequently, our results are likely to reflect the host utilization patterns of S. exigua accurately, comparable to observations in natural field settings.www.nature.com/scientificreports/ The average egg incubation period of S. exigua ranged from 2.7 to 3.5 days across different host plants.Previous investigations on S. exigua raised on synthetic diets indicated an egg incubation span of 2.5 to 5.0 days 23 .However, when reared on various host plants, the egg incubation period lasted between 2.4 to 3.7 days 2,[24][25][26] .Findings unveiled that chickpea larvae exhibited the shortest development period (14.9 days), whereas those consuming castor and maize had notably lengthier durations (24 and 27.1 days, respectively).Similar outcomes were observed in cotton 25,26 and maize 2 , where larval development time ranged from 10 to 29.5 days.Results from this study highlight significant variations in the pupal period among host plants, with larvae reared on maize displaying the most extended pupal duration.This finding aligns with previous research 27,28 , which noted considerable diversity in pupal durations.The nutritional quality provided by a host crop, particularly during the larval stage, primarily influences the biological parameters of any insect population 16 .
The host plant influenced the survival rate of S. exigua during the pupal stage, with the highest survival rate noted on chickpea (84.8%) and the lowest on maize (22.2%).Interestingly, our results indicated that S. exigua survived on all hosts except chilli.The differential survival rates could be attributed to variations in nutrient and biochemical constituents, including primary and secondary metabolites, among crops.These variances may affect the developmental parameters and fitness of S. exigua by altering digestibility and essential nutrient composition 22 .For instance, research by Meade and Hare 29 found survival rates of S. exigua until pupation ranging from 40 to 100% on chrysanthemum and from 27.5 to 82.5% on celery 9 .Differential survival rates reflect the susceptibility of cultivars to pest infestation 29 .The pupal weights of S. exigua were highest on chickpea (89.6 mg) and lowest on maize (30.8 mg).Farahani et al. 30 reported a similar range of pupal weights (73 to 88.1 mg) for S. exigua females on different soybean varieties, consistent with our findings 13 .Abdullah et al. 24 also observed a mean pupal weight of 78.70 mg when rearing S. exigua on an artificial diet.
The larval and pupal stages of S. exigua exhibited the highest growth index on chickpea (5.7 and 9.2, respectively), accompanied by the lowest larval (16.4) and pupal (15.3) mortality rates.This indicates that chickpea is the most favorable host plant for S. exigua.It provides essential nutrients conducive to their growth and development, resulting in shorter developmental periods and increased survival rates.Setamou et al. 31 emphasized that food quality can be accessed through the growth index (GI), which considers survival rate and development time.Greenberg et al. 21observed that higher survival rates and shorter development times correlated with elevated growth index values, indicating superior food quality.Conversely, on maize hybrid DHM117, the larval (1.7) and pupal (0.9) stages of S. exigua experienced the highest percentage of mortality and lower growth index values, suggesting inferior food quality.Generally, lepidopteran larvae consuming highly nutritious food demonstrate faster growth rates and complete development than those feeding on low-nutrient food sources 17 .This study ranks the host crops for S. exigua growth and development: as chickpea, castor, sunflower, blackgram, cotton, groundnut, greengram, and maize.Chilli was identified as the least suitable host for S. exigua, inhibiting their development and survival beyond the third instar larval stage.Variations in the nutritional quality of the host plants utilized by S. exigua larvae could account for the observed differences.
In our study, we observed notable discrepancies in the adult lifespan of S. exigua depending on the host plants, with females generally exhibiting longer lifespan than males, mainly when reared on groundnut, blackgram, and chickpea instead of castor.These findings align with prior research by Khalid Ahmed et al. 27 and Saeed et al. 8,9 .Farahani et al. 26 also documented prolonged female longevity on Z. mays and G. hirsutum.While it is commonly observed that females tend to outlive males in many species, there are inconsistencies across studies.For instance, some studies indicate that male S. exigua may have longer lifespan than females, while others find no significant sex-based differences in longevity 25,28,32 .This variability underscores the complexity of S. exigua's biology and highlights the necessity for further research to understand the factors influencing its development and survival comprehensively.The fecundity of S. exigua varied significantly among the different host plants tested; more eggs were laid when raised on chickpea (2066.1 ± 15.2 eggs/female), while the fewest eggs were laid on maize (286.5 ± 3.82 eggs/female), representing a substantial difference of 1700 eggs.Similar fecundity values on major crops were reported by several researchers 24,33 ; however, lower fecundity values were recorded on off-season or alternate hosts 25 .The nutritional quality significantly influences the egg-laying capacity of female insects 16 .Consistent with the 'mother knows best' hypothesis, it could be speculated that female moths of S. exigua exhibit selective preferences for laying eggs on hosts that offer enhanced nutritional benefits to their offspring.However, in some cases, female moths may choose host plants that do not necessarily ensure optimal fitness for their offspring 34 .
The higher intrinsic rate of increase (r m ) observed in chickpea (0.22 ± 0.0010) was attributed to accelerated development (leading to a shorter generation time), enhanced survivorship, and increased fecundity rates.A high r m value indicates a higher susceptibility of a host plant to insect feeding.In contrast, a low value, as evidenced in maize (0.10 ± 0.0013), suggests that the host plant species possess some level of resistance or tolerance to the pest.Consequently, our findings underscore the substantial growth potential of S. exigua under favorable conditions.In their examination of life table parameters of this pest across various host plants, Greenberg et al. 21observed that the r m value was highest on pigweed (0.264) and lowest on cabbage (0.156).Discrepancies may arise due to physiological variations among host plant cultivars, genetic disparities from laboratory rearing, or geographic variability within pest populations.
Furthermore, our results suggest that maize is a less hospitable host for S. exigua than those examined by Greenberg et al. 21.Our study unveiled that the highest net reproductive rate (R 0 ) of S. exigua was documented on chickpea (846.39 ± 18.22), while the lowest R 0 value was observed on maize (59.50 ± 2.06).Greenberg et al. 21eported slightly lower net reproductive rates for S. exigua, ranging from 139.3 to 596.0 on cabbage and pigweed.Similarly, within the range of 64.53 to 377.73, the lowest R 0 value was recorded on various sorghum varieties.Hence, our findings suggest that the net reproductive rate of S. exigua in chickpea surpasses previous reports by other researchers.Maize displayed the lengthiest generation time (T) at 42.16 ± 0.129 days, whereas chickpea exhibited the shortest at 29.88 days.Naseri et al. 35 explored the reproductive performance of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and reported findings akin to ours 28 .Population doubling on sunflower occurred every 3.56 days, compared to 7.22 days on maize.Host suitability is influenced by various factors, including nutrient content, secondary substances, and the insect's digestive and assimilative capabilities 36,37 .To deepen our understanding of insect-plant interactions, fundamental biochemical studies are essential for isolating and identifying phytochemicals that impede the proliferation of S. exigua populations on off-season hosts.This research may aid in elucidating pest population dynamics on different host cultivars, facilitating the implementation of management strategies to maintain pest populations below economic injury thresholds.

Conclusions
Our research offers valuable insights into the suitability of various host plants for the development, longevity, and survival of S. exigua.Chickpea and sunflower emerged as the most favorable host plants, providing optimal food quality, followed by castor, blackgram, greengram, groundnut, cotton, and maize.The observed differences in the developmental pattern of S. exigua across these resources likely stem from their distinct nutritional profiles and metabolite compositions, impacting the insects' physiology.Our findings suggest that strategies like intercropping, mixed cropping, or crop sequencing with less suitable hosts could influence S. exigua population dynamics and reduce its prevalence.Nevertheless, further field-based research is essential to deepen our understanding of this pest's adaptation to diverse environments and host plants, facilitating the development of effective management practices.

Incidence of S. exigua on different crops and weeds
Field surveys were conducted in eleven mandals of the Prakasam district, i.e., Darsi, Kurichedu, Addanki, Tallur, Mundlamuru, Markapuram, Pedaraveedu, Cumbum, Chirala, J. Panguluru and Marturu during the kharif and post rainy season.During the survey, the incidence of S. exigua on different crops and weeds was recorded randomly in each mandal in three villages.Each sample estimate was based on five locations (fields) in each village, and at each location, 25 plants were randomly selected for each cultivated crop.Each location was treated as one replication, and there were fifteen replicates for each sample (five locations and three villages) in each mandal.During the survey, sampling was also done from weed plants available nearby or within the cultivated crop fields.Data was recorded on several larvae of S. exigua on 25 randomly selected plants and the extent of foliage damage on a 1-9 scale (1 ≤ 10% leaf area damaged and 9 ≥ 80% leaf area damaged).The observations were recorded during the vegetative, flowering, and pod formation stages in their respective crops (Supplementary Tables 1 and 2).After suitable transformations, the data was subjected to analysis of variance and compared based on the least significant difference (LSD) at P = 0.05.

Maintenance of stock culture and studies on biology of S. exigua
To initiate the laboratory culture, S. exigua larvae collected from the field were utilized and reared on their respective host plants in a glasshouse for host conditioning.The lifecycle and fecundity of S. exigua were investigated using various host plants, including Chickpea (var.NBeG The study involved observing the duration of different developmental stages of S. exigua from egg to adult in a laboratory setting.Adults emerging from the respective hosts were placed in a mating chamber (20 cm diameter × 30 cm depth) and provided a 10% honey solution for feeding.Freshly laid egg masses were collected, and each cohort of eggs was placed in labelled plastic Petri dishes (10 cm diameter × 1 cm depth) with a hole in the top cover covered with aluminium wire mesh for aeration.To assess the suitability of different host plants, each host plant was treated as a treatment and replicated 50 times in a randomized design.Upon hatching, each newly emerged larva was individually transferred to a plastic container (9.5 cm top diameter × 6.5 cm bottom diameter × and 12.5 cm high) with a 4 cm diameter ventilated hole in the lid covered with muslin cloth.The larva was fed fresh leaves from each tested host plant until pupation.Moulting was determined by observing the detached head capsule from the newly moulted larva, which was preserved in 70% alcohol to determine the number of instars.After the final moulting stage, the container was filled with vermiculite for pupation, with each larva considered a replication.
The number of days taken to complete each instar was recorded for each cole crop.Other biological and reproductive parameters, such as larval duration, pupal duration, pupal weight, percent pupation, adult emergence, oviposition, pre-and post-oviposition periods, and fecundity, were recorded daily.After adult emergence, pairs of male and female moths (with 20-25 replications) were released in an oviposition chamber covered with fine mesh netting for ventilation.The moths were provided with a 10% honey solution, and test plants were excised and placed in disposable cups at the 3-4 leaf stage as an oviposition substrate to record daily fecundity.The growth index (GI) was calculated by dividing the survival rate of the immature stage by the development time 2 .

Statistical analysis
The biological and reproductive data were analyzed by one-way analysis of variance (ANOVA), followed by a comparison of the means with least significant difference (LSD) test at α = 0.05 using the online statistical software WASP-Web Agri Stat Package 2.0.The life tables of both the pests were constructed by using 'TWOSEX-MS Chart' software.According to the age-stage, two-sex life table principle 38,39 and method 40 , the following parameters viz., Age-stage-specific survival rates (S xj ): S xj = n xj n 01 , age-specific survival rate (l x ): l x = m j=1 S xj ,

Table 4 .
Influence of different host plants on the development of Spodoptera exigua.Means accompanied by the same letter in the same rows are not significantly different at P < 0.05 based on DMRT.Host plants Mean (± SE) of development stages of S. exigua Pre-imaginal developmental period (days) Total life cycle period (days) Overall survival (

Figure 1 .
Figure 1.Age-stage-specific survival rate (S xj ) of Spodoptera exigua on different host plants.

Figure 2 .
Figure 2. Age-stage life expectancy (e xj ) of Spodoptera exigua on different host plants.

Figure 3 .
Figure 3. Age-stage reproductive value (V xj ) of Spodoptera exigua on different host plants.

Figure 6 .
Figure 6.Reproductive value (v x ) of Spodoptera exigua on different host plants.

Table 1 .
Off-season survival of Spodoptera exigua and the extent of damage in different crops in the Prakasam district.# Damage rating (1 ≤ 10% leaf area damaged and 9 ≥ 80% leaf area damaged).*Figures in parenthesis are square root transformed values.**Figures in parenthesis are arc sine transformed values.In a column, means followed by a common letter (s) are not significantly different by DMRT (P = 0.05).

Table 2 .
Longevity of immature stages of Spodoptera exigua reared on different host plants.Means accompanied by the same letter in the same rows are not significantly different at P < 0.05 based on DMRT.

Table 3 .
Longevity of adult stage of Spodoptera exigua reared on different host plants.Means accompanied by the same letter in the same rows are not significantly different at P < 0.05 based on DMRT.Males emerged first, and a day later, females emerged.Egg laying started on 2nd day after the release.

Table 6
presents the intrinsic rate of increase (r), finite rate of increase (lambda), net reproductive rate (R 0 ), gross reproduction rate (GRR), mean generation time (T), and doubling time (DT) of S. exigua on various crops.Among the crops studied, chickpea exhibited the highest intrinsic rate of increase (0.22 ± 0.0010), finite rate of

Table 6 .
Population growth parameters of Spodoptera exigua (mean ± SE) on eight different host plants.Means followed by different letters in the same column are significantly different.Standard errors were estimated using 100,000 bootstrap resampling.